Differences between CAFs and their paired NCF from adjacent colonic mucosa reveal functional heterogeneity of CAFs, providing prognostic information

Molecular Oncology

Volumn 8, Issue 7, 2014, Pages 1290-1305

  Berdiel Acer, Mireia ^a   Sanz Pamplona, Rebeca ^a   Calon, Alexandre ^b   Cuadras, Daniel ^a   Berenguer, Antoni ^a   Sanjuan, Xavier ^c   Paules, Maria José ^c   Salazar, Ramon ^a   Moreno, Victor ^a   Batlle, Eduard ^b   Villanueva, Alberto ^a   Molleví, David G ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

Author keywords

Biomarker; Carcinoma associated fibroblasts; Colorectal; Microenvironment; Stroma

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER PROGNOSIS; CARCINOMA ASSOCIATED FIBROBLAST; CELL CYCLE REGULATION; CELL HETEROGENEITY; CELL INTERACTION; CELL MIGRATION; CELL POPULATION; CLINICAL ARTICLE; CLONOGENESIS; COLON MUCOSA; COLORECTAL CANCER CELL LINE; COLORECTAL CARCINOMA; COMPUTER MODEL; CONTROLLED STUDY; DOWN REGULATION; ESOPHAGUS CANCER; FIBROBLAST; FOCAL ADHESION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LUNG CANCER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROSTATE CANCER; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; COLON; COLORECTAL NEOPLASMS; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; PROGNOSIS;

ANIMALS; CELLS, CULTURED; COLON; COLORECTAL NEOPLASMS; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE, NUDE; PROGNOSIS;

EID: 84908505808     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.04.006     Document Type: Article

References (37)

1. Bauer M., Su G., Casper C., He R., Rehrauer W., Friedl A. Heterogeneity of gene expression in stromal fibroblasts of human breast carcinomas and normal breast. Oncogene 2010, 29:1732-1740.
2. Berdiel-Acer M., Bohem M.E., Lopez-Doriga A., Vidal A., Salazar R., Martinez-Iniesta M., Santos C., Sanjuan X., Villanueva A., Mollevi D.G. Hepatic carcinoma-associated fibroblasts promote an adaptative response in colorectal cancer cells that inhibit proliferation and apoptosis: nonresistant cells die by nonapoptotic cell death. Neoplasia 2011, 13:931-946.
3. Bissell M.J., Hall H.G., Parry G. How does the extracellular matrix direct gene expression?. J.Theor. Biol. 1982, 99:31-68.
4. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 2011, 17:320-329.
5. Calon A., Espinet E., Palomo-Ponce S., Tauriello D.V., Iglesias M., Cespedes M.V., Sevillano M., Nadal C., Jung P., Zhang X.H., Byrom D., Riera A., Rossell D., Mangues R., Massague J., Sancho E., Batlle E. Dependency of colorectal cancer on a TGF-beta-driven program in stromal cells for metastasis initiation. Cancer Cell 2012, 22:571-584.
6. Chang H.Y., Chi J.T., Dudoit S., Bondre C., van de Rijn M., Botstein D., Brown P.O. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:12877-12882.
7. Chang H.Y., Sneddon J.B., Alizadeh A.A., Sood R., West R.B., Montgomery K., Chi J.T., van de Rijn M., Botstein D., Brown P.O. Gene expression signature of fibroblast serum response predicts human cancer progression: similarities between tumors and wounds. PLoS Biol. 2004, 2:E7.
8. Cirri P., Chiarugi P. Cancer associated fibroblasts: the dark side of the coin. Am. J. Cancer Res. 2012, 1:482-497.
9. Costea D.E., Hills A., Osman A.H., Thurlow J., Kalna G., Huang X., Pena Murillo C., Parajuli H., Suliman S., Kulasekara K.K., Johannessen A.C., Partridge M. Identification of two distinct carcinoma-associated fibroblast subtypes with differential tumor-promoting abilities in oral squamous cell carcinoma. Cancer Res. 2013, 73:3888-3901.
10. de Kruijf E.M., van Nes J.G., van de Velde C.J., Putter H., Smit V.T., Liefers G.J., Kuppen P.J., Tollenaar R.A., Mesker W.E. Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res. Treat. 2011, 125:687-696.
11. De Robertis M., Massi E., Poeta M.L., Carotti S., Morini S., Cecchetelli L., Signori E., Fazio V.M. The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies. J.Carcinogenesis 2011, 10:9.
12. de Sousa E.M.F., Colak S., Buikhuisen J., Koster J., Cameron K., de Jong J.H., Tuynman J.B., Prasetyanti P.R., Fessler E., van den Bergh S.P., Rodermond H., Dekker E., van der Loos C.M., Pals S.T., van de Vijver M.J., Versteeg R., Richel D.J., Vermeulen L., Medema J.P. Methylation of cancer-stem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 2011, 9:476-485.
13. Decoster L., Wauters I., Vansteenkiste J.F. Vaccination therapy for non-small-cell lung cancer: review of agents in phase III development. Ann. Oncol. 2012, 23:1387-1393.
14. Elenbaas B., Weinberg R.A. Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp. Cell Res. 2001, 264:169-184.
15. Guo X., Oshima H., Kitmura T., Taketo M.M., Oshima M. Stromal fibroblasts activated by tumor cells promote angiogenesis in mouse gastric cancer. J.Biol. Chem. 2008, 283:19864-19871.
16. Hawinkels L.J., Paauwe M., Verspaget H.W., Wiercinska E., van der Zon J.M., van der Ploeg K., Koelink P.J., Lindeman J.H., Mesker W., ten Dijke P., Sier C.F. Interaction with colon cancer cells hyperactivates TGF-beta signaling in cancer-associated fibroblasts. Oncogene 2014, 33:97-107.
17. Hawsawi N.M., Ghebeh H., Hendrayani S.F., Tulbah A., Al-Eid M., Al-Tweigeri T., Ajarim D., Alaiya A., Dermime S., Aboussekhra A. Breast carcinoma-associated fibroblasts and their counterparts display neoplastic-specific changes. Cancer Res. 2008, 68:2717-2725.
18. Herrera M., Islam A.B., Herrera A., Martin P., Garcia V., Silva J., Garcia J.M., Salas C., Casal I., Garcia de Herreros A., Bonilla F., Pena C. Functional heterogeneity of Cancer-associated fibroblasts from human colon tumors shows specific prognostic gene expression signature. Clin. Cancer Res. 2013, 19:5914-5926.
19. Huijbers A., Tollenaar R.A., v Pelt G.W., Zeestraten E.C., Dutton S., McConkey C.C., Domingo E., Smit V.T., Midgley R., Warren B.F., Johnstone E.C., Kerr D.J., Mesker W.E. The proportion of tumor-stroma as a strong prognosticator for stage II and III colon cancer patients: validation in the VICTOR trial. Ann. Oncol. 2013, 24:179-185.
20. Hwang R.F., Moore T., Arumugam T., Ramachandran V., Amos K.D., Rivera A., Ji B., Evans D.B., Logsdon C.D. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008, 68:918-926.
21. Jorissen R.N., Gibbs P., Christie M., Prakash S., Lipton L., Desai J., Kerr D., Aaltonen L.A., Arango D., Kruhoffer M., Orntoft T.F., Andersen C.L., Gruidl M., Kamath V.P., Eschrich S., Yeatman T.J., Sieber O.M. Metastasis-associated gene expression changes predict poor outcomes in patients with Dukes stage B and C Colorectal Cancer. Clin. Cancer Res. 2009, 15:7642-7651.
22. Liu X., Nugoli M., Laferriere J., Saleh S.M., Rodrigue-Gervais I.G., Saleh M., Park M., Hallett M.T., Muller W.J., Giguere V. Stromal retinoic acid receptor beta promotes mammary gland tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:774-779.
23. Louie E., Chen X.F., Coomes A., Ji K., Tsirka S., Chen E.I. Neurotrophin-3 modulates breast cancer cells and the microenvironment to promote the growth of breast cancer brain metastasis. Oncogene 2013, 32:4064-4077.
24. Navab R., Strumpf D., Bandarchi B., Zhu C.Q., Pintilie M., Ramnarine V.R., Ibrahimov E., Radulovich N., Leung L., Barczyk M., Panchal D., To C., Yun J.J., Der S., Shepherd F.A., Jurisica I., Tsao M.S. Prognostic gene-expression signature of carcinoma-associated fibroblasts in non-small cell lung cancer. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7160-7165.
25. Nemunaitis J., Nemunaitis M., Senzer N., Snitz P., Bedell C., Kumar P., Pappen B., Maples P.B., Shawler D., Fakhrai H. Phase II trial of Belagenpumatucel-L, a TGF-beta2 antisense gene modified allogeneic tumor vaccine in advanced non small cell lung cancer (NSCLC) patients. Cancer Gene Ther. 2009, 16:620-624.
26. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tlsty T.D., Cunha G.R. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999, 59:5002-5011.
27. Orimo A., Gupta P.B., Sgroi D.C., Arenzana-Seisdedos F., Delaunay T., Naeem R., Carey V.J., Richardson A.L., Weinberg R.A. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005, 121:335-348.
28. Peng Q., Zhao L., Hou Y., Sun Y., Wang L., Luo H., Peng H., Liu M. Biological characteristics and genetic heterogeneity between carcinoma-associated fibroblasts and their paired normal fibroblasts in human breast cancer. PLoS One 2013, 8:e60321.
29. Quante M., Tu S.P., Tomita H., Gonda T., Wang S.S., Takashi S., Baik G.H., Shibata W., Diprete B., Betz K.S., Friedman R., Varro A., Tycko B., Wang T.C. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19:257-272.
30. Rickelt S., Winter-Simanowski S., Noffz E., Kuhn C., Franke W.W. Upregulation of plakophilin-2 and its acquisition to adherens junctions identifies a novel molecular ensemble of cell-cell-attachment characteristic for transformed mesenchymal cells. Int. J. Cancer 2009, 125:2036-2048.
31. Smith J.J., Deane N.G., Wu F., Merchant N.B., Zhang B., Jiang A., Lu P., Johnson J.C., Schmidt C., Bailey C.E., Eschrich S., Kis C., Levy S., Washington M.K., Heslin M.J., Coffey R.J., Yeatman T.J., Shyr Y., Beauchamp R.D. Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology 2010, 138:958-968.
32. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15545-15550.
33. Torres S., Bartolome R.A., Mendes M., Barderas R., Fernandez-Acenero M.J., Pelaez-Garcia A., Pena C., Lopez-Lucendo M., Villar-Vazquez R., de Herreros A.G., Bonilla F., Casal J.I. Proteome profiling of cancer-associated fibroblasts identifies novel proinflammatory signatures and prognostic markers for colorectal cancer. Clin. Cancer Res. 2013, 19:6006-6019.
34. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:5116-5121.
35. Wilson C.L., Miller C.J. Simpleaffy: a BioConductor package for Affymetrix Quality Control and data analysis. Bioinformatics 2005, 21:3683-3685.
36. Worthley D.L., Giraud A.S., Wang T.C. Stromal fibroblasts in digestive cancer. Cancer Microenviron. 2010, 3:117-125.
37. Zhang C., Fu L., Fu J., Hu L., Yang H., Rong T.H., Li Y., Liu H., Fu S.B., Zeng Y.X., Guan X.Y. Fibroblast growth factor receptor 2-positive fibroblasts provide a suitable microenvironment for tumor development and progression in esophageal carcinoma. Clin. Cancer Res. 2009, 15:4017-4027.